competitive advantage over many co-occurring native plants, and economic impacts of plant invasions, it is important to yet this competitive success is not completely understood.

increase our understanding of the physiological and environ- While prolific seed production, high germination rates, and mental factors that influence the invasive potential of plant easy dispersal of its small seeds have been hypothesized to species to facilitate preventative and remediation efforts.

facilitate the spread of this species (Ma1 et al., 1992; Mullin, Lythrum salicaria (purple loosestrife), a herbaceous peren- 19981, the continued success of L. salicaria also depends on nial introduced from Europe and Asia, is thought to have ar- its successful growth following establishment. Though it has rived in North America during the early 1800s (Thompson, been widely hypothesized that a lack of natural herbivores has 1991). Since its introduction, this species has become partic- given this species (Thompson, Stuckey, and Thompson, 1987; ularly widespread across wetland, marshy, and riparian habi- Rendall, 1989; Galatowitsch, Anderson, and Ascher, 1999) and tats in the northern tier states and provinces of North America.

other invasive species (RejmLnek, 1996; Mack et al., 2000) a The spread of this species, along with that of other invasive competitive growth advantage over co-occurring native spe- plants, has altered the vegetation of many North American cies, recent studies have indicated the vigor of L. salicaria wetlands (Galatowitsch, Anderson, and Ascher, 1999), result- cannot be explained entirely by either a lack of herbivory ing in the decline of species diversity and the extinction of (Rachich and Reader, 1999; Willis and Blossey, 1999) or a some rare species (Moore and Keddy, 1989). Invasions of L.

The authors thank the A.W. Mellon Foundation for providing the principal

ing invasions of "salicaria (Thompson, Stuckey3 and Thomp

funding support for this research; A. Peterson, W. Schuster, K. Brown, D. Peteet, X. Wang, V. Engel, and M. Potosnak for their ideas and assistance Son, 1987; Mullin, 19981, and collectivel~, many studies have during the design and process of this experiment, as well as their comments indicated there are positive correlations between disturbance on earlier drafts of this manuscript; B. Mace, A. Thompson, and A. Arch for and other species invasions in environments ranging from wet- their technical assistance; the Black Rock Forest Consortium for use of the

landS (e.g., ~ ~ et al., 1999) to grasslands (e.g., R ~ ~ b ~~

field sites: and the anonymous reviewers of this manuscript. This is Lamont-

ence the invasiveness of L. salicaria and numerous other ~lant species; ecosystem modeling results support this conclusion (Zalba et al., 2000). Yet the invasive species and their neigh- boring noninvasive species sharing these disturbed environ- ments are subiect to the same environmental conditions. re- gardless of thi nature of the disturbance. Some components of plant physiology andlor morphology may, therefore, also influence the invasive potential of plant species by enabling them to establish populations capable of outcompeting other species in disturbed environments.

As a quantifiable measurement of the energy invested by a plant to construct biomass, construction cost (CC) can be re- lated to both resource-use efficiency (Williams et al., 1987; Griffin, 1994) and growth rates (Lambers and Poorter, 1992; Poorter and Bergkotte, 1992; Griffin, Thomas, and Strain, 1993; Griffin, 1994; Poorter and Villar, 1997), with high CC typically being associated with slow-growing species (Lamb- ers and Poorter, 1992; Poorter and Bergkotte, 1992; Griffin, Thomas, and Strain, 1993; Griffin, 1994; Poorter and Villar, 1997). Since every plant species has a resource requirement below which it cannot perform the functions necessary to grow and spread (Tilman, 1982), it has been hypothesized that a relatively low resource requirement could increase the com- petitive ability of plant species (Tilman, 1999). As it relates to CC, the resource requirement of a species could be influ- enced by the amount of energy required to perform growth functions, such that a plant requiring less energy to construct biomass may require less resources to generate that energy than a plant with more energetically expensive functions. Since a quantitative understanding of how different plants gain and allocate resources likely will facilitate predictions of their success in any given environment (Mooney, 1972) and plant energetics can be related to resource use, we consider CC as a general approach to evaluating invasive potential.

Researchers who recently studied 30 invasive and 34 native species in Hawaii found overall lower leaf CC for the invasive vs. native species (Baruch and Goldstein, 1999). Comparing native and invasive C, grasses in Venezuela, another study concluded a similar occurrence of low leaf CC in invasive plants when compared to their native counterparts (Baruch and Gomez, 1996). Given these recent findings and the association of CC with resource-use efficiency and growth rates, we hy- pothesize the invasiveness of L. salicaria over co-occurring native plants may be facilitated by relatively low energy re- quirements for leaf construction. Thus, L. salicaria may pro- duce more photosynthetic leaf surface area and/or grow faster with lower energy expense to outcompete co-occurring native species. We investigated our hypothesis by comparing the leaf CC and related resource characteristics of field-collected L. salicaria and the five most abundant co-occurring native spe- cies along disturbed, dammed areas of three man-made ponds located in the Black Rock Forest, Cornwall, New York, USA.

MATERIALS AND METHODS

Leaf material-Vegetation surveys were conducted during the summer of 1999 around disturbed, dammed sections of three ponds-Upper Reservoir, Aleck Meadow Reservoir, and Sphagnum Pond-located in the Black Rock Forest, Cornwall, New York, USA. All three sites were in cleared areas of the forest and rece~ved direct sunlight. Along these dams, I-m2 plots were marked every 10 m along the pond banks, with the location of the first plot randomly assigned. The edge of the pond marked the boundary of one side of each plot. In total, 33 plots were marked. All dicot plant individuals within these plots were identified and counted. For L. salicaria, which can have many stems per individual (Ma1 et al., 1992), stems rising from the same rootstock were counted as one individual plant. Species relative abundance levels were determined on a density basis as the total number of individuals of each species divided by the total number of quadrants (in individuals per square meter). We have chosen to use this measure of abundance because it attests to the growth success as well as the establishment success of species.

Young, fully expanded sun leaves from one observably healthy individual of L. salicaria and the five most abundant co-occurring native species were collected from every plot where the respective species was present. To ensure enough leaf material was obtained for our analyses, -50 cm2 of leaf material was collected from each individual plant. Leaves were processed through a portable area meter (Model LI-3000A, LI-COR, Lincoln, Nebraska, USA) and then dried in a 60°C oven (Model 20 GC, Quincy Lab, Chicago, Illinois, USA) for 48 h and weighed to determine leaf mass per unit area (LMA) (in grams per square meter) for each individual. Following this measurement, all dried leaves were ground into a fine powder using a ball mill (Cianflone Scientific Instruments, Pittsburgh, Pennsylvania, USA) and stored with a des- iccant to maintain dryness for construction cost analysis.

Leaf energy and resource investment-Organic nitrogen (N) (in grams per gram leaf dry mass) and carbon (C) (in grams per gram leaf dry mass) content of two 1-2 mg samples of leaf powder from each individual were determined using an elemental analyzer (ANCA-SL, ANCA, Crewe, UK). The duplicate samples for each individual were averaged. To calculate N and C per unit leaf area (in grams per square meter), these values were multiplied by the LMA for each individual.

Ash content (Ash) (in grams per gram leaf dry mass) was measured for each individual by burning preweighed leaf powder samples in a 400°C muffle furnace (Model 51844, Lindberg, Watertown, Wisconsin, USA) for 6 h to obtain ash and then dividing the ash mass by the sample mass. To obtain ash- free heats of combustion (H,) (in kilojoules per gram leaf dry mass), three 6-20 mg pellets were pressed of the leaf powder from each individual. The pellets were combusted using a modified Phillipson microbomb calorimeter (Phillipson, 1964) (Gentry Instruments, Aiken, South Carolina, USA) cali- brated with 6-20 mg benzoic acid standards of known energy values. The H, values obtained for the triplicate pellets for each plant were then averaged.

The simplest measurement of CC involves quantifying the amount of re- sources allocated to a given vegetative structure's formation, which can be estimated accurately from measurements of H,, Ash, and N content (Williams et al., 1987). The following equation (from Williams et al., 1987) was used to calculate CC as the amount of glucose required to synthesize plant biomass (equivalent to grams glucose per gram leaf dry mass): CC = [(0.06968AHc -0.065)(1 -Ash) + 7.5(kN/14.0067)](1/E,); where k is the oxidation state of the nitrogen substrate and E, is the growth efficiency. In terms of its deviation from 100%, E, represents the fraction of cost required to provide reductant that is not incorporated into biomass (Penning de Vries, Brunsting, and van Laar, 1974). Penning de Vries, Brunsting, and van Laar (1974) cal- culated E, as 0.87. Since k is +5 for nitrate and -3 for ammonium and the form of N was not known in our samples, CC for each individual was cal- culated twice, once with k = 5 and once with k = -3, providing a range of possible N substrate-dependent CC values. To calculate leaf CC per unit leaf area (equivalent to grams glucose per square meter), these values were mul- tiplied by the LMA for each individual. Species means were obtained for all measured factors by averaging the values of all individuals for each species.

Statistical analyses-After homogeneity of sample variances was verified using a Levene statistic test, a one-way analysis of variance (ANOVA) model adjusted for unbalanced experimental design (in which species was defined as the fixed independent variable) was used to compare means between spe- cies for all measured leaf variables (SPSS for Windows, release 7.5.1, 1996, SPSS, Chicago, Illinois, USA). Mean values were considered significantly different if P 5 0.05. When ANOVA results were significant, least significant difference (LSD) post-hoc analysis was performed to further compare species means. Linear regressions were made to determine the relationship between mean leaf CC and other leaf variables for all species. The average of the leaf

TABLE1. Summary of one-way analysis of variance (ANOVA) results for all measured leaf physiological variables, where species was considered the fixed independent variable.

Leaf variable Sum of squares df Mean square F P

Density (individuals/m2) Between groups Within groups Total

cca(g/g) Between groups Within groups Total

CC (g/m2) Between groups Within groups

Total

LMAb (g/m2) Between groups Within groups Total

C (mg/g) Between groups Within groups Total C (g/m2) Between groups Within groups Total N (mglg) Between groups Within groups Total N (g/m2) Between groups Within groups Total

C:N Between groups Within groups Total

a CC = construction cost.LMA = leaf mass per unit area.

CC values considering ammonium and nitrate each as the primary source of leaf N were used in regression analysis.

RESULTS

Relative abundance, area- and mass-based leaf CC, leaf N and C, and C :N were all significantly different between sam- pled species (Table 1). Overall, 39 species were identified along the dammed areas of the pond perimeters. Of the species sampled, Parthenocissus quinquefolia (Virginia creeper), L. salicaria, and Erigeron philadelphicus (common fleabane) were significantly more abundant than Asclepias syriaca (common milkweed), Spiraea latifolia (meadowsweet), and Solidago graminifolia (lance-leaved goldenrod) (Fig. 1). Collectively, these species included a vine (P. quinquefolia), a shrub (Spirea latifolia), and four herbs. All are common in the region of this study, and all but L. salicaria are native to North Amer- ica. Sample sizes were reflective of the relative abundance of the species and were consistent for all analyses (n = 19 for

Fig. 1. Abundance of invasive L. salicaria and the five most abundant co-occurring species along dammed sections of three ponds in the Black Rock Forest, New York, USA. Error bars represent 1 SE of the mean. Means shown below the same letter are not significantly different at the P 5 0.05 level of significance.

the primary source of organic N, was generally lower in the more relatively abundant species and higher in the less rela- tively abundant species (Fig. 2). Both P. quinquefolia and L. salicaria, as well as Spirea latifolia, had significantly lower mass-based leaf CC than the other sampled species, with least- abundant Solidago grarninifolia exhibiting the greatest mass- based leaf CC (Fig. 2A). When expressed per unit area, P. quinquefolia and L. salicaria exhibited significantly lower mean leaf CC values than all other sampled species, including Spirea latifolia, while both Solidago grarninifolia and A. syr- iaca had the statistically highest mean area-based leaf CC. (Fig. 2B). Linear regression analysis revealed a significant negative correlation between area-based mean leaf CC and species relative abundance (Fig. 3), but only a weak degree of correlation when leaf CC was expressed per unit leaf dry mass (r2= 0.31).

Other leaf characteristics also varied significantly according to species relative abundance. In general, LMA increased with increasing relative abundance, with P. quinquefolia and L. salicaria exhibiting significantly lower mean LMA values than the other sampled species (Table 2). Both of these species also had significantly lower mean leaf C per unit leaf area than the other sampled species, though L. salicaria alone exhibited the significantly lowest mass-based leaf C value. Conversely, the three least abundant species, A. syriaca, Spirea latifolia, and Solidago grarninifolia, exhibited the highest area- and mass- based mean leaf C values (Table 2). Expressed per unit leaf area, mean leaf N was significantly lower in P. quinquefolia,

N appeared to exhibit an interspecific trend opposite to that of mass-based mean leaf N, with P. quinquefolia, L. salicaria,

SALICARIA

Fig. 2. Mean leaf CC of L. salicaria and the five most abundant co-occurring species in the study sites (A) expressed per unit leaf dry mass and (B) expressed per unit leaf area. Construction cost was calculated considering each ammonium (open bars) and nitrate (shaded bars) as the primary source of leaf

N. Species are listed along the x-axis in order of decreasing abundance (left to right). Error bars represent 1 SE of the mean. Means shown below the same letter are not significantly different at the P 5 0.05 level of significance.

A combination of these leaf characteristics seemed to be CC in this study suggests processes dependent on leaf surface associated with area-based leaf CC, while leaf CC expressed area may influence competitive success of these species to per unit dry leaf mass was not correlated significantly with some extent. In fact, we found LMA to be slightly more any of the measured leaf variables. Specifically, both LMA strongly correlated with species relative abundance than is (Fig. 4A) and area-based leaf C (Fig. 4B) were moderately area-based leaf CC in this study (r2= 0.81). However, because correlated with area-based mean leaf CC, while mean leaf N LMA is not a cause but rather the result of a change in phys-

per unit leaf area was strongly correlated with this factor (Fig. iology, while leaf CC may be considered a more mechanistic 4C). However, there was no significant degree of correlation approach to understanding plant growth, we emphasize leaf between mean leaf C : N and area-based leaf CC.

CC and related factors. Here, a positive correlation between LMA and area-based DISCUSSION mean leaf CC (Fig. 4A) illustrates the association of leaf CC and leaf thickness or cell density. Typically, plants with a high Since leaves are the primary site of photosynthetic carbon LMA have been found to contain more lignin (Austin and gain, leaf CC, in particular, could have profound impacts on Vitousek, 1998; Groeneveld, Bergkotte, and Lambers, 1998) species growth and abundance. Specifically, a relatively low and cell-wall components (Groeneveld, Bergkotte, and Lamb- area-based leaf CC that allows the construction of more leaf ers, 1998), which tend to be energetically expensive. In our surface area with low energetic expense, such as that exhibited study, this association seemed characteristic of two of the less by both invasive L. salicaria and weedy P. quinquefolia in

this study, may provide some species with a competitive ad- abundant species, A. syriaca and Solidago graminifolia, which vantage over others. More indirectly, low energy requirements exhibited relatively high mean LMA values associated with for leaf construction could allow such species to invest more both high mass- and area-based leaf CC, while both P. quinenergy in other strategies, such as reproductive efforts or root quefolia and L. salicara exhibited the opposite characteristics. growth. The relatively low mean LMA of the most abundant sam- Area-based leaf CC estimates provide information on pro- pled species in this study (Table 2) could indicate these species cesses influenced by leaf surface area, such as those driven by have a higher capacity for light interception and carbon assim- light interception or those limited by diffusion to the plant ilation with a limited amount of energetic expense, while rel-

TABLE2. Leaf resource investment of six species along pond banks in the Black Rock Forest. Leaf mass per unit area (LMA), organic carbon

(C) and nitrogen content (N), and carbon-to-nitrogen molar ratio (C : N) of invasive Lythrum salicaria and its five most abundant neighboring species within the study sites. Species are presented in order of decreasing abundance (left to right). Values presented are species means tl SE. Values followed by the same superscript letter are not significantly different at the P = 0.05 level of significance.

atively higher mean LMA could have the opposite effect in co-occurring species. Though photosynthesis was not measured in our study, researchers who examined photosynthesis of invasive plants with lower LMA and leaf CC than co-occurring native plants concluded the invasive species had overall higher average rates of mass-based photosynthesis (Baruch and Goldstein, 1999).

Nitrogen, which is contained in many of the more expensive biochemical plant compounds (Penning de Vries, Brunsting, and van Laar, 1974) such as proteins and amino acids (Williams et al., 1987), typically exhibits a positive correlation with leaf CC (Miller, Eddleman, and Kramer, 1990; Sims and Pearcy, 1991; Griffin, Thomas, and Strain, 1993; Griffin, Winner, and Strain, 1996). The relatively high mass-based leaf N and low mass-based leaf CC in both L. salicaria and P. quinquefolia in this study suggests these species have a low energetic expense per unit N, which could increase photosynthetic capacity at minimal cost. Yet the strong positive correlation between area-based leaf N and CC (Fig. 4C) reflects the influence of interspecific differences in LMA. Like area-based leaf N, leaf C also seemed to be influenced by LMA (Fig. 4B). Relating both N and C content, the significantly low leaf C : N of L. salicaria could indicate reduced herbivory defense in the form of low amounts of structural carbon compounds, such as cellulose and lignin (Herms and Mattson, 1992), which have an energetic cost.

In L. salicaria, low leaf CC may be indicative of high resource-use efficiency and growth rates, both of which could facilitate its invasiveness. As it correlates with species abundance in this study, leaf CC could provide a useful evaluation of invasive potential that may be applicable in other settings. While past research has sugge~tedthere may be little interspecific variation in this factor (e.g., Merino, 1987; Chapin, 1989; Williams, Field, and Mooney, 1989), a more recent review has found a twofold range in mass-based leaf CC and an even greater range in area-based leaf CC between species

(Griffin, 1994). Our findings, while contributing only a small piece to the complex puzzle of species invasions, support those of a very limited number of other studies examining leaf CC and species invasiveness (e.g., Baruch and Gomez, 1996; Baruch and Goldstein, 1999).

COST OF LYTHRUM

While more specific physiological and morphological char- acteristics may contribute to the relative competitive ability of a species, it often is difficult to draw conclusions regarding the influence of these specific characteristics on invasive po- tential due to a lack of commonality. For example, while some invasive species may have high seed production or the ability to fix nitrogen, other invasive species may not share these characteristics. However, since every growth strategy has an energy consequence, energy can be considered a basic unit of comparison between organisms (Griffin, 1994). As such, CC measurements reflect specific growth strategies, while allow- ing for a more general comparison of resource-use efficiency between species. We propose examining leaf CC of native and invasive species in other settings to further evaluate the ap- plication of this factor for assessing invasive potential. Fur- thermore, we suggest evaluating CC measurements for other plant structures, such as roots, stems, and seeds, to gain insight into patterns of energy use and resource allocation within in- vasive and co-occurring native plants.

BARUCH, Z., AND J. A. GOMEZ. 1996. Dynamics of energy and nutrient con- centration and construction cost in a native and two alien C, grasses from two neotropical savannas. Plant and Soil 181: 175-184.